Recruitment and dissociation of nonhomologous end joining proteins at a DNA double-strand break in Saccharomyces cerevisiae

Genetics

Volumn 178, Issue 3, 2008, Pages 1237-1249

  Wu, Dongliang ^a   Topper, Leana M ^a   Wilson, Thomas E ^a,b  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b 2065 BSRB ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DEOXYRIBONUCLEOPROTEIN; DOUBLE STRANDED DNA; FUNGAL PROTEIN; HETERODIMER; KU ANTIGEN; NEJ1 PROTEIN; NONHOMOLOGOUS END JOINING PROTEIN; POLYDEOXYRIBONUCLEOTIDE SYNTHASE; RAD50 PROTEIN; UNCLASSIFIED DRUG; ADENOSINE TRIPHOSPHATE; CELL NUCLEUS ANTIGEN; DNA BINDING PROTEIN; MULTIPROTEIN COMPLEX; NEJ1 PROTEIN, S CEREVISIAE; POLYDEOXYRIBONUCLEOTIDE SYNTHASE (ATP); SACCHAROMYCES CEREVISIAE PROTEIN;

ARTICLE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DISSOCIATION; DNA REPAIR; DOUBLE STRANDED DNA BREAK; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN SECRETION; SACCHAROMYCES CEREVISIAE; YEAST; ENZYMOLOGY; FUNGAL GENE; GENETIC RECOMBINATION; GENETICS; METABOLISM; POLYMERASE CHAIN REACTION; PROMOTER REGION; SOUTHERN BLOTTING; TIME;

SACCHAROMYCES CEREVISIAE;

ADENOSINE TRIPHOSPHATE; ANTIGENS, NUCLEAR; BLOTTING, SOUTHERN; CHROMATIN IMMUNOPRECIPITATION; DNA BREAKS, DOUBLE-STRANDED; DNA LIGASES; DNA-BINDING PROTEINS; GENES, FUNGAL; MULTIPROTEIN COMPLEXES; POLYMERASE CHAIN REACTION; PROMOTER REGIONS (GENETICS); PROTEIN BINDING; RECOMBINATION, GENETIC; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TIME FACTORS;

EID: 45149104841     PISSN: 00166731     EISSN: 00166731     Source Type: Journal    
DOI: 10.1534/genetics.107.083535     Document Type: Article

References (66)

1. AHNESORG, P., and S. P. JACKSON, 2007 The non-homologous endjoining protein Nej1p is a target of the DNA damage checkpoint. DNA Repair 6: 190-201.
2. ANDERSON, D. E., K. M. TRUJILLO, P. SUNG and H. P. ERICKSON, 2001 Structure of the Rad50 x Mre11 DNA repair complex from Saccharomyces cerevisiae by electron microscopy. J. Biol. Chem. 276: 37027-37033.
3. APARICIO, O., J. V. GEISBERG, E. SEKINGER, A. YANG, Z. MOQTADERI et al., 2005 Chromatin immunoprecipitation for determining the association of proteins with specific genomic sequences in vivo, pp. 21.3.1-21.3.33 in Current Protocols in Molecular Biology, edited by F. M. AUSUBEL, R. BRENT, R. E. KINGSTON, D. D. MOORE, J. G. SEIDMAN, J. A. SMITH and K. STRUHL. John Wiley & Sons, New York.
4. AYLON, Y., B. LIEFSHITZ and M. KUPIEC, 2004 The CDK regulates repair of double-strand breaks by homologous recombination during the cell cycle. EMBO J. 23: 4868-4875.
5. BOEGER, H., J. GRIESENBECK, J. S. STRATTAN and R. D. KORNBERG, 2003 Nucleosomes unfold completely at a transcriptionally active promoter. Mol. Cell 11: 1587-1598.
6. BOULTON, S. J., and S. P. JACKSON, 1998 Components of the Ku-dependent non-homologous end-joining pathway are involved in telomeric length maintenance and telomeric silencing. EMBO J. 17: 1819-1828.
7. BRACHMANN, C. B., A. DAVIES, G. J. COST, E. CAPUTO, J. LI et al., 1998 Designer deletion strains derived from Saccharomyces cerevisiae S288C: a useful set of strains and plasmids for PCR-mediated gene disruption and other applications. Yeast 14: 115-132.
8. BRESSAN, D. A., B. K. BAXTER and J. H. PETRINI, 1999 The Mre11-Rad50-Xrs2 protein complex facilitates homologous recombination-based double-strand break repair in Saccharomyces cerevisiae. Mol. Cell. Biol. 19: 7681-7687.
9. CALSOU, P., C. DELTEIL, P. FRIT, J. DROUET and B. SALLES, 2003 Coordinated assembly of Ku and p460 subunits of the DNA-dependent protein kinase on DNA ends is necessary for XRCC4-ligase IV recruitment. J. Mol. Biol. 326: 93-103.
10. CHEN, L., K. TRUJILLO, W. RAMOS, P. SUNG and A. E. TOMKINSON, 2001 Promotion of Dnl4-catalyzed DNA end-joining by the Rad50/Mre11/Xrs2 and Hdf1/Hdf2 complexes. Mol. Cell 8: 1105-1115.
11. CHEN, L., K. M. TRUJILLO, S. VAN KOMEN, D. H. ROH, L. KREJCI et al., 2005 Effect of amino acid substitutions in the Rad50 ATP binding domain on DNA double strand break repair in yeast. J. Biol. Chem. 280: 2620-2627.
12. CONNELLY, J. C., and D. R. LEACH, 2002 Tethering on the brink: the evolutionarily conserved Mre11-Rad50 complex. Trends Biochem. Sci. 27: 410-418.
13. DALEY,J. M.,P.L.PALMBOS,D.WUandT.E. WILSON,2005 Nonhomologous end joining in yeast. Annu. Rev. Genet. 39: 431-451.
14. D'AMOURS, D., and S. P. JACKSON, 2002 The mre11 complex: at the crossroads of DNA repair and checkpoint signalling. Nat. Rev. Mol. Cell Biol. 3: 317-327.
15. DESHPANDE, R. A., and T. E. WILSON, 2007 Modes of interaction among yeast Nej1, Lif1 and Dnl4 proteins and comparison to human XLF, XRCC4 and Lig4. DNA Repair 6: 1507-1516.
16. DORE, A. S., N. FURNHAM, O. R. DAVIES, B. L. SIBANDA, D. Y. CHIRGADZE et al., 2006 Structure of an Xrcc4-DNA ligase IV yeast ortholog complex reveals a novel BRCT interaction mode. DNA Repair 5: 362-368.
17. DUDASOVA, Z., A. DUDAS and M. CHOVANEC, 2004 Non-homologous end-joining factors of Saccharomyces cerevisiae. FEMS Microbiol. Rev. 28: 581-601.
18. FRANK-VAILLANT, M., and S. MARCAND, 2001 NHEJ regulation by mating type is exercised through a novel protein, Lif2p, essential to the ligase IV pathway. Genes Dev. 15: 3005-3012.
19. FRANK-VAILLANT, M., and S. MARCAND, 2002 Transient stability of DNA ends allows nonhomologous end joining to precede homologous recombination. Mol. Cell 10: 1189-1199.
20. FURUSE, M., Y. NAGASE, H. TSUBOUCHI, K. MURAKAMI-MUROFUSHI, T. SHIBATA et al., 1998 Distinct roles of two separable in vitro activities of yeast Mre11 in mitotic and meiotic recombination. EMBO J. 17: 6412-6425.
21. GRIFFITH, A. J., P. R. BLIER, T. MIMORI and J. A. HARDIN, 1992 Ku polypeptides synthesized in vitro assemble into complexes which recognize ends of double-stranded DNA. J. Biol. Chem. 267: 331-338.
22. HABER, J. E., 1995 In vivo biochemistry: physical monitoring of recombination induced by site-specific endonucleases. BioEssays 17: 609-620.
23. HERRMANN, G., T. LINDAHL and P. SCHAR, 1998 Saccharomyces cerevisiae LIF1: a function involved in DNA double-strand break repair related to mammalian XRCC4. EMBO J. 17: 4188-4198.
24. HOPFNER, K. P., A. KARCHER, L. CRAIG, T. T. WOO, J. P. CARNEY et al., 2001 Structural biochemistry and interaction architecture of the DNA double-strand break repair Mre11 nuclease and Rad50-ATPase. Cell 105: 473-485.
25. HSU, H. L., S. M. YANNONE and D. J. CHEN, 2002 Defining interactions between DNA-PK and ligase IV/XRCC4. DNA Repair 1: 225-235.
26. IRA, G., A. PELLICIOLI, A. BALIJJA, X. WANG, S. FIORANI et al., 2004 DNA end resection, homologous recombination and DNA damage checkpoint activation require CDK1. Nature 431: 1011-1017.
27. IVANOV, E. L., N. SUGAWARA, C. I. WHITE, F. FABRE and J. E. HABER, 1994 Mutations in XRS2 and RAD50 delay but do not prevent mating-type switching in Saccharomyces cerevisiae. Mol. Cell. Biol. 14: 3414-3425.
28. KARATHANASIS, E., and T. E. WILSON, 2002 Enhancement of Saccharomyces cerevisiae end-joining efficiency by cell growth stage but not by impairment of recombination. Genetics 161: 1015-1027.
29. KROGH, B. O., B. LLORENTE, A. LAMAND L. S. SYMINGTON, 2005 Mutations in Mre11 phosphoesterase motif I that impair Saccharomyces cerevisiae Mre11-Rad50-Xrs2 complex stability in addition to nuclease activity. Genetics 171: 1561-1570.
30. LEE, S. E., J. K. MOORE, A. HOLMES, K. UMEZU, R. D. KOLODNER et al., 1998 Saccharomyces Ku70, mre11/rad50 and RPA proteins regulate adaptation to G2/M arrest after DNA damage. Cell 94: 399-409.
31. LI, S., and M. J. SMERDON, 2002 Nucleosome structure and repair of N-methylpurines in the GAL1-10 genes of Saccharomyces cerevisiae. J. Biol. Chem. 277: 44651-44659.
32. LISBY, M., J. H. BARLOW, R. C. BURGESS and R. ROTHSTEIN, 2004 Choreography of the DNA damage response: spatiotemporal relationships among checkpoint and repair proteins. Cell 118: 699-713.
33. LONGTINE, M. S., A. MCKENZIE, III, D. J. DEMARINI, N. G. SHAH, A. WACH et al., 1998 Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14: 953-961.
34. MARI, P. O., B. I. FLOREA, S. P. PERSENGIEV, N. S. VERKAIK, H. T. BRUGGENWIRTH et al., 2006 Dynamic assembly of end-joining complexes requires interaction between Ku70/80 and XRCC4. Proc. Natl. Acad. Sci. USA 103: 18597-18602.
35. MCCORMICK, S. P., J. K. NG, S. TAYLOR, L. M. FLYNN, R. E. HAMMER et al., 1995 Mutagenesis of the human apolipoprotein B gene in a yeast artificial chromosome reveals the site of attachment for apolipoprotein(a). Proc. Natl. Acad. Sci. USA 92: 10147-10151.
36. MILNE, G. T., S. JIN, K. B. SHANNON and D. T. WEAVER, 1996 Mutations in two Ku homologs define a DNA end-joining repair pathway in Saccharomyces cerevisiae. Mol. Cell. Biol. 16: 4189-4198.
37. MODESTI, M., J. E. HESSE and M. GELLERT, 1999 DNA binding of XRCC4 protein is associated with V(D)J recombination but not with stimulation of DNA ligase IV activity. EMBO J. 18: 2008-2018.
38. MOREAU, S., J. R. FERGUSON and L. S. SYMINGTON, 1999 The nuclease activity of Mre11 is required for meiosis but not for mating type switching, end joining, or telomere maintenance. Mol. Cell. Biol. 19: 556-566.
39. MOREIRA, J. M., W. HORZ and S. HOLMBERG, 2002 Neither Reb1p nor poly(dA*T) elements are responsible for the highly specific chromatin organization at the ILV1 promoter. J. Biol. Chem. 277: 3202-3209.
40. NAYAK, T., E. SZEWCZYK, C. E. OAKLEY, A. OSMANI, L. UKIL et al., 2006 A versatile and efficient gene-targeting system for Aspergillus nidulans. Genetics 172: 1557-1566.
41. NICK MCELHINNY, S. A., C. M. SNOWDEN, J. MCCARVILLE and D. A. RAMSDEN, 2000 Ku recruits the XRCC4-ligase IV complex to DNA ends. Mol. Cell. Biol. 20: 2996-3003.
42. NINOMIYA, Y., K. SUZUKI, C. ISHII and H. INOUE, 2004 Highly efficient gene replacements in Neurospora strains deficient for nonhomologous end-joining. Proc. Natl. Acad. Sci. USA 101: 12248-12253.
43. PALMBOS, P. L., J. M. DALEY and T. E. WILSON, 2005 Mutations of the Yku80 C terminus and Xrs2 FHA domain specifically block yeast nonhomologous end joining. Mol. Cell. Biol. 25: 10782-10790.
44. PETERSON, K. R., Q. L. LI, C. H. CLEGG, T. FURUKAWA, P. A. NAVAS et al., 1995 Use of yeast artificial chromosomes (YACs) in studies of mammalian development: production of beta-globin locus YAC mice carrying human globin developmental mutants. Proc. Natl. Acad. Sci. USA 92: 5655-5659.
45. RAVINDRA, A., K. WEISS and R. T. SIMPSON, 1999 High-resolution structural analysis of chromatin at specific loci: Saccharomyces cerevisiae silent mating-type locus HMRa. Mol. Cell. Biol. 19: 7944-7950.
46. REAGAN, M. S., and J. E. MAJORS, 1998 The chromatin structure of the GAL1 promoter forms independently of Reb1p in Saccharomyces cerevisiae. Mol. Gen. Genet. 259: 142-149.
47. REINKE, H., and W. HORZ, 2003 Histones are first hyperacetylated and then lose contact with the activated PHO5 promoter. Mol. Cell 11: 1599-1607.
48. REVY, P., L. MALIVERT and J. P. DE VILLARTAY, 2006 Cernunnos-XLF, a recently identified non-homologous end-joining factor required for the development of the immune system. Curr. Opin. Allergy Clin. Immunol. 6: 416-420.
49. SHIM, E. Y., J. L. MA, J. H. OUM, Y. YANEZ and S. E. LEE, 2005 The yeast chromatin remodeler RSC complex facilitates end joining repair of DNA double-strand breaks. Mol. Cell. Biol. 25: 3934-3944.
50. SHIM, E. Y., S. J. HONG, J. H. OUM, Y. YANEZ, Y. ZHANG et al., 2007 RSC mobilizes nucleosomes to improve accessibility of repair machinery to the damaged chromatin. Mol. Cell. Biol. 27: 1602-1613.
51. SHIMA, H., M. SUZUKI and M. SHINOHARA, 2005 Isolation and characterization of novel xrs2 mutations in Saccharomyces cerevisiae. Genetics 170: 71-85.
52. SUNG, P., K. M. TRUJILLO and S. VAN KOMEN, 2000 Recombination factors of Saccharomyces cerevisiae. Mutat. Res. 451: 257-275.
53. SYMINGTON, L. S., 2002 Role of RAD52 epistasis group genes in homologous recombination and double-strand break repair. Microbiol. Mol. Biol. Rev. 66: 630-670.
54. SYMINGTON, L. S., and W. D. HEYER, 2006 Some disassembly required: role of DNA translocases in the disruption of recombination intermediates and dead-end complexes. Genes Dev. 20: 2479-2486.
55. TRUJILLO, K. M., D. H. ROH, L. CHEN, S. VAN KOMEN, A. TOMKINSON et al., 2003 Yeast xrs2 binds DNA and helps target Rad50 and Mre11 to DNA ends. J. Biol. Chem. 278: 48957-48964.
56. TSUKAMOTO, Y., A. K. TAGGART and V. A. ZAKIAN, 2001 The role of the Mre11-Rad50-Xrs2 complex in telomerase-mediated lengthening of Saccharomyces cerevisiae telomeres. Curr. Biol. 11: 1328-1335.
57. TSUKUDA, T., A. B. FLEMING, J. A. NICKOLOFF and M. A. OSLEY, 2005 Chromatin remodelling at a DNA double-strand break site in Saccharomyces cerevisiae. Nature 438: 379-383.
58. USUI, T., T. OHTA, H. OSHIUMI, J. TOMIZAWA, H. OGAWA et al., 1998 Complex formation and functional versatility of Mre11 of budding yeast in recombination. Cell 95: 705-716.
59. VALENCIA, M., M. BENTELE, M. B. VAZE, G. HERRMANN, E. Kraus et al., 2001 NEJ1 controls non-homologous end joining in Saccharomyces cerevisiae. Nature 414: 666-669.
60. WALKER, J. R., R. A. CORPINA and J. GOLDBERG, 2001 Structure of the Ku heterodimer bound to DNA and its implications for double-strand break repair. Nature 412: 607-614.
61. WEISS, K., and R. T. SIMPSON, 1998 High-resolution structural analysis of chromatin at specific loci: Saccharomyces cerevisiae silent mating type locus HMLalpha. Mol. Cell. Biol. 18: 5392-5403.
62. WILSON, T. E., 2007 Nonhomologous end-joining: mechanisms, conservation and relationship to illegitimate recombination, pp. 487-513 in Molecular Genetics of Recombination (Topics in Current Genetics), edited by A. AGUILERA and R. ROTHSTEIN. Springer-Verlag, Berlin/Heidelberg, Germany/New York.
63. WILSON, T. E., U. GRAWUNDER and M. R. LIEBER, 1997 Yeast DNA ligase IV mediates non-homologous DNA end joining. Nature 388: 495-498.
64. WILTZIUS, J. J., M. HOHL, J. C. FLEMING and J. H. PETRINI, 2005 The Rad50 hook domain is a critical determinant of Mre11 complex functions. Nat. Struct. Mol. Biol. 12: 403-407.
65. WU, P. Y., P. FRIT, L. MALIVERT, P. REVY, D. BIARD et al., 2007 Interplay between cernunnos-XLF and NHEJ proteins at DNA ends in the cell. J. Biol. Chem. 282: 31937-31943.
66. ZHANG, Y., M. L. HEFFERIN, L. CHEN, E. Y. SHIM, H. M. TSENG et al., 2007 Role of Dnl4-Lif1 in nonhomologous end-joining repair complex assembly and suppression of homologous recombination. Nat. Struct. Mol. Biol. 14: 639-646.